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The ability of terrestrial Oligochaeta to survive in ultramafic soils and the assessment of toxicity at different levels of organisation

Maleri, Rudolf A. (2006-12)

Thesis (PhD (Botany and Zoology)) -- University of Stellenbosch, 2006.

Thesis

Metals are natural elements of the earth crust usually present at low concentrations in all soils.
Although many metals such as cobalt, copper, iron and zinc are essential to living organisms, at
elevated concentrations most metals are toxic to organisms living in and on soils. Elevated
concentrations of metals are caused either by anthropogenic deposition following remobilisation
from the earth crust or are of natural origin.
Ultramafic soils do not only pose unfavourable living conditions such as drought and poor organic
content, these soils are also characterized by extremely high concentrations of a range of metals
known to be toxic under normal circumstances. Ultramafic soils are of high ecological importance
as a high proportion of endemic organisms, especially plants, live on these soils.
As it is known that earthworms do occur in ultramafic soils, the aims of the present study were to
investigate the abilities of earthworms to survive in these soils and the influences of elevated
chromium, cobalt, copper, manganese and nickel levels.
For the evaluation of the metal background conditions, soils originating from ultramafic rocks of the
Barberton Greenstone Belt, Mpumalanga, South Africa were collected and different fractions
representing different levels of bioavailability were analyzed for arsenic, chromium, cobalt, copper,
manganese and nickel. To assess the mobile, readily available metal fraction, i.e. Ca2+-
exchangeable metal cations, a 0.01 mol/L CaCl2 extraction was performed. To investigate the
mobilisable metal fraction, representing the amount of easily remobilisable complexed and
carbonated metal ions, a DTPA (di-ethylene-triamine-pentaacetic acid) extraction was conducted.
In relation to non-ultramafic or anthropogenic contaminated soils, a far lower proportion of metals
were extractable by the above mentioned extraction methods.
To investigate the availability and effects of these metals on earthworms, two ecophysiologically
different species were employed. Aporrectodea caliginosa and Eisenia fetida were long-term
exposed to the ultramafic soils collected at the Barberton region and a control soil from a location
at Stellenbosch with a known history of no anthropogenic metal contamination. The responses to
the ecological stress originating in the ultramafic soils were measured on different levels of
earthworm organisation. As endpoints affecting population development, cocoon production,
fecundity and viability were evaluated. On individual level, growth, metal body burden and tissue
distribution were investigated. As endpoints on subcellular level, the membrane integrity was
assessed by the neutral red retention assay, the mitochondrial activity was measured by the MTT
colorimetric assay and as a biomarker for the DNA integrity, the comet assay was performed.
Focussing on manganese and nickel, the uptake by E. fetida of these metals was investigated with
the exclusion of soil related properties using an artificial aqueous medium to draw comparisons to
the uptake of these metals in natural soils.
The possible development of resistance towards nickel was tested by exposing pre-exposed (for
more than 10 generations) E. fetida specimens to ultramafic soils with concentrations of more than
4000 mg/kg nickel. The results showed that, except on the endpoint survival, which was less sensitive than all other
bioassays, significant responses to the ultramafic challenge were observed in all earthworm
bioassays and on all levels of organisation. The sensitivity of the responses of the earthworms
towards the ultramafic conditions was not predictable by the level of organisation.
The two species showed different strategies of metal elimination. In A. caliginosa, metals such as
nickel, manganese and chromium were transported to the posterior section and the posterior
section was subsequently pushed off by autotomization. In E. fetida, metals such as chromium and
nickel were sequestered in storage compartments in the coelomic cells or fluid. Other metals, such
as cobalt, were not taken up at elevated concentrations.
Although an increased accumulation of nickel was observed in E. fetida specimens pre-exposed to
nickel, development of resistance or cross resistance was not observed in this species. In contrast,
pre-exposed specimen exposed to elevated concentrations of nickel showed a higher sensitivity in
terms of survival, indicating the absence of acclimatisation or even genetic adaptation.
A comparison of the two species employed indicated that A. caliginosa was less suited for the
assessment of the ultramafic soils due to the high individual variation in metal body burden, the
mass loss observed and the slow reproduction rate even in the control soils. This happened
despite the fact that A. caliginosa was a soil dwelling species supposed to be better adapted to the
soil substrate than the litter dwelling E. fetida.
The toxicity of the ultramafic soils was not necessarily related to total or environmentally available
amounts of the selected metals. Thus, it can be speculated that either these soils contained
unidentified toxicants with resulting interactions between toxicants playing an important role or
earthworms were able to remobilize metals occurring in these soils.
As the singular application of an ecotoxicological endpoint did not give reliable results, especially
seen over the duration of the exposures, it can be concluded that, when studying soils with such a
complex composition, the utilisation of endpoints addressing different levels of organisation is
necessary for the assessment of toxic stress emerging from these ultramafic soils.